Skip to main content

Advertisement

SpringerLink
Log in

The origin and continuing adaptive evolution of chikungunya virus

  • Review
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Chikungunya virus (CHIKV) is the responsible agent of chikungunya fever, a debilitating arthritic disease in humans. CHIKV is endemic in Africa and Asia, although transmission cycles are considerably different on these continents. Before 2004, CHIKV had received little attention, since it was only known to cause localised outbreaks in a limited region with no fatalities. However, the recent global reemergence of CHIKV has caused serious global health problems and shown its potential to become a significant viral threat in the future. Unexpectedly, the reemergence is more rapid and is geographically more extensive, especially due to increased intensity of global travel systems or failure to contain mosquito populations. Another important factor is the successful adaptation of CHIKV to a new vector, the Aedes albopictus mosquito. Ae. albopictus survives in both temperate and tropical climates, thus facilitating CHIKV expansion to non-endemic regions. The continuous spread and transmission of CHIKV pose challenges for the development of effective vaccines and specific antiviral therapies. In this review, we discuss the biology and origin of CHIKV in Africa as well as its subsequent expansion to other parts of the world. We also review the transmission cycle of CHIKV and its continuing adaptation to its mosquito vectors and vertebrate hosts. More-complete understanding of the continuous evolution of CHIKV may help in predicting the emergence of CHIKV strains with possibly greater transmission efficiency in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Young PR (2018) Arboviruses: a family on the move. Adv Exp Med Biol 1062:1–10

    Article  CAS  Google Scholar 

  2. Go YY, Balasuriya UB, Lee CK (2014) Zoonotic encephalitides caused by arboviruses: transmission and epidemiology of alphaviruses and flaviviruses. Clin Exp Vaccine Res 3:58–77

    Article  Google Scholar 

  3. Gould E, Pettersson J, Higgs S, Charrel R, de Lamballerie X (2017) Emerging arboviruses: why today? One Health 4:1–13

    Article  Google Scholar 

  4. Mascarenhas M, Garasia S, Berthiaume P, Corrin T, Greig J, Ng V, Young I, Waddell L (2018) A scoping review of published literature on chikungunya virus. PLoS One 13:e0207554

    Article  Google Scholar 

  5. Deeba F, Haider MSH, Ahmed A, Tazeen A, Faizan MI, Salam N, Hussain T, Alamery SF, Parveen S (2020) Global transmission and evolutionary dynamics of the chikungunya virus. Epidemiol Infect 148:e63

    Article  CAS  Google Scholar 

  6. Wilder-Smith A, Gubler DJ, Weaver SC, Monath TP, Heymann DL, Scott TW (2017) Epidemic arboviral diseases: priorities for research and public health. Lancet Infect Dis 17:e101–e106

    Article  Google Scholar 

  7. Zaid A, Burt FJ, Liu X, Poo YS, Zandi K, Suhrbier A, Weaver SC, Texeira MM, Mahalingam S (2021) Arthritogenic alphaviruses: epidemiological and clinical perspective on emerging arboviruses. Lancet Infect Dis 21:e123–e133

    Article  CAS  Google Scholar 

  8. Khan AH, Morita K, Parquet MDC, Hasebe F, Mathenge EGM, Igarashi A (2002) Complete nucleotide sequence of chikungunya virus and evidence for an internal polyadenylation site. J Gen Virol 83:3075–3084

    Article  CAS  Google Scholar 

  9. Wong KZ, Chu JJH (2018) The interplay of viral and host factors in chikungunya virus infection: targets for antiviral strategies. Viruses 10:294

    Article  Google Scholar 

  10. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA (2010) Glycoprotein organization of chikungunya virus particles revealed by X-ray crystallography. Nature 468:709–712

    Article  CAS  Google Scholar 

  11. Quiroz JA, Malonis RJ, Thackray LB, Cohen CA, Pallesen J, Jangra RK, Brown RS, Hofmann D, Holtsberg FW, Shulenin S, Nyakatura EK, Durnell LA, Rayannavar V, Daily JP, Ward AB, Aman MJ, Dye JM, Chandran K, Diamond MS, Kielian M, Lai JR (2019) Human monoclonal antibodies against chikungunya virus target multiple distinct epitopes in the E1 and E2 glycoproteins. PLoS Pathog 15:e1008061

    Article  Google Scholar 

  12. Chua CL, Sam IC, Merits A, Chan YF (2016) Antigenic variation of East/Central/South African and Asian chikungunya virus genotypes in neutralization by immune sera. PLoS Negl Trop Dis 10:e0004960

    Article  Google Scholar 

  13. Tsetsarkin KA, Chen R, Weaver SC (2016) Interspecies transmission and chikungunya virus emergence. Curr Opin Virol 16:143–150

    Article  Google Scholar 

  14. Valentine MJ, Murdock CC, Kelly PJ (2019) Sylvatic cycles of arboviruses in non-human primates. Parasit Vectors 12:463

    Article  Google Scholar 

  15. Diallo M, Thonnon J, Traore-Lamizana M, Fontenille D (1999) Vectors of chikungunya virus in Senegal: current data and transmission cycles. Am J Trop Med Hyg 60:281–286

    Article  CAS  Google Scholar 

  16. Diallo D, Sall AA, Buenemann M, Chen R, Faye O, Diagne CT, Faye O, Ba Y, Dia I, Watts D, Weaver SC, Hanley KA, Diallo M (2012) Landscape ecology of sylvatic chikungunya virus and mosquito vectors in southeastern Senegal. PLoS Negl Trop Dis 6:e1649

    Article  Google Scholar 

  17. Paupy C, Kassa Kassa F, Caron M, Nkoghe D, Leroy EM (2012) A chikungunya outbreak associated with the vector Aedes albopictus in remote villages of Gabon. Vector Borne Zoonotic Dis 12:167–169

    Article  Google Scholar 

  18. Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI, Graham AL, Lloyd-Smith JO (2017) Pathways to zoonotic spillover. Nat Rev Microbiol 15:502–510

    Article  CAS  Google Scholar 

  19. Powers AM, Brault AC, Tesh RB, Weaver SC (2000) Re-emergence of chikungunya and O'nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J Gen Virol 81:471–479

    CAS  Google Scholar 

  20. Eastwood G, Sang RC, Guerbois M, Taracha ELN, Weaver SC (2017) Enzootic circulation of chikungunya virus in east Africa: serological evidence in non-human Kenyan primates. Am J Trop Med Hyg 97:1399–1404

    Article  Google Scholar 

  21. Althouse BM, Guerbois M, Cummings DAT, Diop OM, Faye O, Faye A, Diallo D, Sadio BD, Sow A, Faye O, Sall AA, Diallo M, Benefit B, Simons E, Watts DM, Weaver SC, Hanley KA (2018) Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal. Nat Commun 9:1046

    Article  Google Scholar 

  22. Raulino R, Thaurignac G, Butel C, Villabona-Arenas CJ, Foe T, Loul S, Ndimbo-Kumugo SP, Mbala-Kingebeni P, Makiala-Mandanda S, Ahuka-Mundeke S, Kerkhof K, Delaporte E, Arien KK, Foulongne V, Mpoudi Ngole E, Peeters M, Ayouba A (2021) Multiplex detection of antibodies to chikungunya, O'nyong-nyong, Zika, Dengue, West Nile and Usutu viruses in diverse non-human primate species from Cameroon and the Democratic Republic of Congo. PLoS Negl Trop Dis 15:e0009028

    Article  CAS  Google Scholar 

  23. Apandi Y, Nazni WA, Noor Azleen AZ, Vythilingam I, Noorazian MY, Azahari AH, Zainah S, Lee HL (2009) The first isolation of chikungunya virus from nonhuman primates in Malaysia. J Gen Mol Virol 1:35–39

    Google Scholar 

  24. Suhana O, Nazni WA, Apandi Y, Farah H, Lee HL, Sofian-Azirun M (2019) Insight into the origin of chikungunya virus in Malaysian non-human primates via sequence analysis. Heliyon 5:e02682

    Article  CAS  Google Scholar 

  25. Sam IC, Chua CL, Rovie-Ryan JJ, Fu JY, Tong C, Sitam FT, Chan YF (2015) Chikungunya virus in macaques, Malaysia. Emerg Infect Dis 21:1683–1685

    Article  CAS  Google Scholar 

  26. Marchette NJ, Rudnick A, Garcia R, MacVean DW (1978) Alphaviruses in Peninusular Malaysia: I. Virus isolations and animal serology. Southeast Asian J Trop Med Public Health 9:317–329

    CAS  Google Scholar 

  27. Inoue S, Morita K, Matias RR, Tuplano JV, Resuello RR, Candelario JR, Cruz DJ, Mapua CA, Hasebe F, Igarashi A, Natividad FF (2003) Distribution of three arbovirus antibodies among monkeys (Macaca fascicularis) in the Philippines. J Med Primatol 32:89–94

    Article  CAS  Google Scholar 

  28. Halstead SB, Udomsakdi S (1966) Vertebrate hosts of chikungunya virus. Bull World Health Organ 35:89

    CAS  Google Scholar 

  29. Vourc'h G, Halos L, Desvars A, Boue F, Pascal M, Lecollinet S, Zientara S, Duval T, Nzonza A, Bremont M (2014) Chikungunya antibodies detected in non-human primates and rats in three Indian Ocean islands after the 2006 ChikV outbreak. Vet Res 45:52

    Article  Google Scholar 

  30. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, Andau M, Spielman A, Gubler DJ (2001) Sylvatic transmission of arboviruses among Bornean orangutans. Am J Trop Med Hyg 64:310–316

    Article  CAS  Google Scholar 

  31. Valentine MJ, Ciraola B, Aliota MT, Vandenplas M, Marchi S, Tenebray B, Leparc-Goffart I, Gallagher CA, Beierschmitt A, Corey T, Dore KM, de Lamballerie X, Wang C, Murdock CC, Kelly PJ (2020) No evidence for sylvatic cycles of chikungunya, dengue and Zika viruses in African green monkeys (Chlorocebus aethiops sabaeus) on St. Kitts, West Indies. Parasit Vectors 13:540

    Article  CAS  Google Scholar 

  32. Moreira-Soto A, Carneiro IO, Fischer C, Feldmann M, Kummerer BM, Silva NS, Santos UG, Souza B, Liborio FA, Valenca-Montenegro MM, Laroque PO, da Fontoura FR, Oliveira AVD, Drosten C, de Lamballerie X, Franke CR, Drexler JF (2018) Limited evidence for infection of urban and peri-urban nonhuman primates with Zika and chikungunya viruses in Brazil. mSphere 3:e00523–e00517

    Article  Google Scholar 

  33. Lourenco-de-Oliveira R, Failloux AB (2017) High risk for chikungunya virus to initiate an enzootic sylvatic cycle in the tropical Americas. PLoS Negl Trop Dis 11:e0005698

    Article  Google Scholar 

  34. Anggraeni YM, Garjito TA, Prihatin MT, Handayani SW, Negari KS, Yanti AO, Hidajat MC, Prastowo D, Satoto TBT, Manguin S, Gavotte L, Frutos R (2021) Fast expansion of the Asian-Pacific genotype of the chikungunya virus in Indonesia. Front Cell Infect Microbiol 11:631508

    Article  CAS  Google Scholar 

  35. Figueiredo LTM (2019) Human urban arboviruses can infect wild animals and jump to sylvatic maintenance cycles in south America. Front Cell Infect Microbiol 9:259

    Article  Google Scholar 

  36. Robinson MC (1955) An epidemic of virus disease in southern province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans R Soc Trop Med Hyg 49:28–32

    Article  CAS  Google Scholar 

  37. Lumsden WH (1955) An epidemic of virus disease in southern province, Tanganyika Territory, in 1952-53. II. General description and epidemiology. Trans R Soc Trop Med Hyg 49:33–57

    Article  CAS  Google Scholar 

  38. Robinson MC (1956) An epidemic of a dengue-like fever in the southern province of Tanganyika. Cent Afr J Med 2:394–396

    CAS  Google Scholar 

  39. Mason PJ, Haddow AJ (1957) An epidemic of virus disease in southern province, Tanganyika Territory, in 1952-53; an additional note on Chikungunya virus isolations and serum antibodies. Trans R Soc Trop Med Hyg 51:238–240

    Article  CAS  Google Scholar 

  40. Ross RW (1956) The Newala epidemic. III. The virus: isolation, pathogenic properties and relationship to the epidemic. J Hyg (Lond) 54:177–191

    Article  CAS  Google Scholar 

  41. Zeller H, Van Bortel W, Sudre B (2016) Chikungunya: its history in Africa and Asia and its spread to new regions in 2013–2014. J Infect Dis 214:S436–S440

    Article  Google Scholar 

  42. Tsetsarkin KA, Chen R, Sherman MB, Weaver SC (2011) Chikungunya virus: evolution and genetic determinants of emergence. Curr Opin Virol 1:310–317

    Article  CAS  Google Scholar 

  43. Lanciotti RS, Ludwig ML, Rwaguma EB, Lutwama JJ, Kram TM, Karabatsos N, Cropp BC, Miller BR (1998) Emergence of epidemic O'nyong-nyong fever in Uganda after a 35-year absence: genetic characterization of the virus. Virology 252:258–268

    Article  CAS  Google Scholar 

  44. Lutwama JJ, Kayondo J, Savage HM, Burkot TR, Miller BR (1999) Epidemic O'Nyong-Nyong fever in southcentral Uganda, 1996–1997: entomologic studies in Bbaale village, Rakai District. Am J Trop Med Hyg 61:158–162

    Article  CAS  Google Scholar 

  45. Cherian SS, Walimbe AM, Jadhav SM, Gandhe SS, Hundekar SL, Mishra AC, Arankalle VA (2009) Evolutionary rates and timescale comparison of chikungunya viruses inferred from the whole genome/E1 gene with special reference to the 2005-07 outbreak in the Indian subcontinent. Infect Genet Evol 9:16–23

    Article  CAS  Google Scholar 

  46. Volk SM, Chen R, Tsetsarkin KA, Adams AP, Garcia TI, Sall AA, Nasar F, Schuh AJ, Holmes EC, Higgs S, Maharaj PD, Brault AC, Weaver SC (2010) Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 84:6497–6504

    Article  CAS  Google Scholar 

  47. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S (2007) A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3:e201

    Article  Google Scholar 

  48. Hammon WM, Rudnick A, Sather GE (1960) Viruses associated with epidemic hemorrhagic fevers of the Philippines and Thailand. Science 131:1102–1103

    Article  CAS  Google Scholar 

  49. Khongwichit S, Chansaenroj J, Thongmee T, Benjamanukul S, Wanlapakorn N, Chirathaworn C, Poovorawan Y (2021) Large-scale outbreak of chikungunya virus infection in Thailand, 2018–2019. PLoS One 16:e0247314

    Article  CAS  Google Scholar 

  50. Chastel C (1963) Human infections in Cambodia by the chikungunya virus or an apparently closely related agent. I. Clinical aspects. Isolations and identification of the viruses. Serology. Bull Soc Pathol Exot Fil 56:892–915

    CAS  Google Scholar 

  51. Khongwichit S, Chansaenroj J, Chirathaworn C, Poovorawan Y (2021) Chikungunya virus infection: molecular biology, clinical characteristics, and epidemiology in Asian countries. J Biomed Sci 28:84

    Article  Google Scholar 

  52. Yergolkar PN, Tandale BV, Arankalle VA, Sathe PS, Sudeep AB, Gandhe SS, Gokhle MD, Jacob GP, Hundekar SL, Mishra AC (2006) Chikungunya outbreaks caused by African genotype, India. Emerg Infect Dis 12:1580–1583

    Article  CAS  Google Scholar 

  53. Porter KR, Tan R, Istary Y, Suharyono W, Sutaryo, Widjaja S, Ma'Roef C, Listiyaningsih E, Kosasih H, Hueston L, McArdle J, Juffrie M (2004) A serological study of chikungunya virus transmission in Yogyakarta, Indonesia: evidence for the first outbreak since 1982. Southeast Asian J Trop Med Public Health 35:408–415

    Google Scholar 

  54. Salje H, Cauchemez S, Alera MT, Rodriguez-Barraquer I, Thaisomboonsuk B, Srikiatkhachorn A, Lago CB, Villa D, Klungthong C, Tac-An IA, Fernandez S, Velasco JM, Roque VG Jr, Nisalak A, Macareo LR, Levy JW, Cummings D, Yoon IK (2016) Reconstruction of 60 years of chikungunya epidemiology in the Philippines demonstrates episodic and focal transmission. J Infect Dis 213:604–610

    Article  Google Scholar 

  55. Harapan H, Michie A, Mudatsir M, Nusa R, Yohan B, Wagner AL, Sasmono RT, Imrie A (2019) Chikungunya virus infection in Indonesia: a systematic review and evolutionary analysis. BMC Infect Dis 19:243

    Article  Google Scholar 

  56. Sergon K, Njuguna C, Kalani R, Ofula V, Onyango C, Konongoi LS, Bedno S, Burke H, Dumilla AM, Konde J, Njenga MK, Sang R, Breiman RF (2008) Seroprevalence of chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. Am J Trop Med Hyg 78:333–337

    Article  Google Scholar 

  57. Renault P, Solet JL, Sissoko D, Balleydier E, Larrieu S, Filleul L, Lassalle C, Thiria J, Rachou E, de Valk H, Ilef D, Ledrans M, Quatresous I, Quenel P, Pierre V (2007) A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. Am J Trop Med Hyg 77:727–731

    Article  Google Scholar 

  58. Renault P, Josseran L, Pierre V (2008) Chikungunya-related fatality rates, Mauritius, India, and Reunion Island. Emerg Infect Dis 14:1327

    Article  Google Scholar 

  59. Josseran L, Paquet C, Zehgnoun A, Caillere N, Le Tertre A, Solet JL, Ledrans M (2006) Chikungunya disease outbreak, Reunion Island. Emerg Infect Dis 12:1994–1995

    Article  Google Scholar 

  60. Pongsiri P, Auksornkitti V, Theamboonlers A, Luplertlop N, Rianthavorn P, Poovorawan Y (2010) Entire genome characterization of chikungunya virus from the 2008–2009 outbreaks in Thailand. Trop Biomed 27:167–176

    CAS  Google Scholar 

  61. Wanlapakorn N, Thongmee T, Linsuwanon P, Chattakul P, Vongpunsawad S, Payungporn S, Poovorawan Y (2014) Chikungunya outbreak in Bueng Kan Province, Thailand, 2013. Emerg Infect Dis 20:1404–1406

    Article  CAS  Google Scholar 

  62. Duong V, Andries AC, Ngan C, Sok T, Richner B, Asgari-Jirhandeh N, Bjorge S, Huy R, Ly S, Laurent D, Hok B, Roces MC, Ong S, Char MC, Deubel V, Tarantola A, Buchy P (2012) Reemergence of chikungunya virus in Cambodia. Emerg Infect Dis 18:2066–2069

    Article  Google Scholar 

  63. Sam IC, Chan YF, Chan SY, Loong SK, Chin HK, Hooi PS, Ganeswrie R, Abubakar S (2009) Chikungunya virus of Asian and Central/East African genotypes in Malaysia. J Clin Virol 46:180–183

    Article  CAS  Google Scholar 

  64. Maha MS, Susilarini NK, Hariastuti NI, Subangkit (2015) Chikungunya virus mutation, Indonesia, 2011. Emerg Infect Dis 21:379–381

    Article  CAS  Google Scholar 

  65. Badar N, Salman M, Ansari J, Aamir U, Alam MM, Arshad Y, Mushtaq N, Ikram A, Qazi J (2020) Emergence of chikungunya virus, Pakistan, 2016–2017. Emerg Infect Dis 26:307–310

    Article  Google Scholar 

  66. Pan J, Fang C, Yan J, Yan H, Zhan B, Sun Y, Liu Y, Mao H, Cao G, Lv L, Zhang Y, Chen E (2019) Chikungunya fever outbreak, Zhejiang Province, China, 2017. Emerg Infect Dis 25:1589–1591

    Article  Google Scholar 

  67. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A, group Cs (2007) Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840–1846

    Article  CAS  Google Scholar 

  68. Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, Cordioli P, Angelini P, Venturelli C, Merialdi G, Dottori M (2008) Chikungunya virus in Aedes albopictus, Italy. Emerg Infect Dis 14:852–854

    Article  Google Scholar 

  69. Venturi G, Di Luca M, Fortuna C, Remoli ME, Riccardo F, Severini F, Toma L, Del Manso M, Benedetti E, Caporali MG, Amendola A, Fiorentini C, De Liberato C, Giammattei R, Romi R, Pezzotti P, Rezza G, Rizzo C (2017) Detection of a chikungunya outbreak in Central Italy, August to September 2017. Euro Surveill 22:17–00646

    Article  Google Scholar 

  70. Rezza G (2018) Chikungunya is back in Italy: 2007–2017. J Travel Med. https://doi.org/10.1093/jtm/tay004

    Article  Google Scholar 

  71. Grandadam M, Caro V, Plumet S, Thiberge JM, Souares Y, Failloux AB, Tolou HJ, Budelot M, Cosserat D, Leparc-Goffart I, Despres P (2011) Chikungunya virus, southeastern France. Emerg Infect Dis 17:910–913

    Article  Google Scholar 

  72. Cao-Lormeau VM, Musso D (2014) Emerging arboviruses in the Pacific. Lancet 384:1571–1572

    Article  Google Scholar 

  73. van Bortel W, Dorleans F, Rosine J, Blateau A, Rousset D, Matheus S, Leparc-Goffart I, Flusin O, Prat C, Cesaire R, Najioullah F, Ardillon V, Balleydier E, Carvalho L, Lemaitre A, Noel H, Servas V, Six C, Zurbaran M, Leon L, Guinard A, van den Kerkhof J, Henry M, Fanoy E, Braks M, Reimerink J, Swaan C, Georges R, Brooks L, Freedman J, Sudre B, Zeller H (2014) Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. Euro Surveill 19:20759

    Google Scholar 

  74. Nhan TX, Claverie A, Roche C, Teissier A, Colleuil M, Baudet JM, Cao-Lormeau VM, Musso D (2014) Chikungunya virus imported into French Polynesia, 2014. Emerg Infect Dis 20:1773–1774

    Article  Google Scholar 

  75. Aubry M, Teissier A, Huart M, Merceron S, Vanhomwegen J, Mapotoeke M, Mariteragi-Helle T, Roche C, Vial AL, Teururai S, Sicard S, Paulous S, Despres P, Manuguerra JC, Mallet HP, Imrie A, Musso D, Deparis X, Cao-Lormeau VM (2018) Seroprevalence of dengue and chikungunya virus antibodies, French Polynesia, 2014–2015. Emerg Infect Dis 24:558–561

    Article  Google Scholar 

  76. Aubry M, Cao-Lormeau VM (2019) History of arthropod-borne virus infections in French Polynesia. New Microbes New Infect 29:100513

    Article  CAS  Google Scholar 

  77. Aubry M, Teissier A, Roche C, Richard V, Yan AS, Zisou K, Rouault E, Maria V, Lastere S, Cao-Lormeau VM, Musso D (2015) Chikungunya outbreak, French Polynesia, 2014. Emerg Infect Dis 21:724–726

    Article  CAS  Google Scholar 

  78. Sanjuan R, Domingo-Calap P (2016) Mechanisms of viral mutation. Cell Mol Life Sci 73:4433–4448

    Article  CAS  Google Scholar 

  79. Domingo E, Perales C (2019) Viral quasispecies. PLoS Genet 15:e1008271

    Article  CAS  Google Scholar 

  80. Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178

    Article  CAS  Google Scholar 

  81. Tong JC, Simarmata D, Lin RT, Renia L, Ng LF (2010) HLA class I restriction as a possible driving force for chikungunya evolution. PLoS One 5:e9291

    Article  Google Scholar 

  82. Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney MC, Lavenir R, Pardigon N, Reynes JM, Pettinelli F, Biscornet L, Diancourt L, Michel S, Duquerroy S, Guigon G, Frenkiel MP, Brehin AC, Cubito N, Despres P, Kunst F, Rey FA, Zeller H, Brisse S (2006) Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med 3:e263

    Article  Google Scholar 

  83. Coffey LL, Vignuzzi M (2011) Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J Virol 85:1025–1035

    Article  CAS  Google Scholar 

  84. Coffey LL, Beeharry Y, Borderia AV, Blanc H, Vignuzzi M (2011) Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci USA 108:16038–16043

    Article  CAS  Google Scholar 

  85. Weiss CM, Liu H, Riemersma KK, Ball EE, Coffey LL (2020) Engineering a fidelity-variant live-attenuated vaccine for chikungunya virus. NPJ Vaccines 5:97

    Article  CAS  Google Scholar 

  86. Arias-Goeta C, Moutailler S, Mousson L, Zouache K, Thiberge JM, Caro V, Rougeon F, Failloux AB (2014) Chikungunya virus adaptation to a mosquito vector correlates with only few point mutations in the viral envelope glycoprotein. Infect Genet Evol 24:116–126

    Article  CAS  Google Scholar 

  87. Yuan M, Lu T, Li C, Lu L (2013) The evolutionary rates of HCV estimated with subtype 1a and 1b sequences over the ORF length and in different genomic regions. PLoS One 8:e64698

    Article  CAS  Google Scholar 

  88. Anishchenko M, Bowen RA, Paessler S, Austgen L, Greene IP, Weaver SC (2006) Venezuelan encephalitis emergence mediated by a phylogenetically predicted viral mutation. Proc Natl Acad Sci USA 103:4994–4999

    Article  CAS  Google Scholar 

  89. Brault AC, Powers AM, Ortiz D, Estrada-Franco JG, Navarro-Lopez R, Weaver SC (2004) Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci USA 101:11344–11349

    Article  CAS  Google Scholar 

  90. Ebel GD, Carricaburu J, Young D, Bernard KA, Kramer LD (2004) Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 71:493–500

    Article  CAS  Google Scholar 

  91. Moudy RM, Meola MA, Morin LL, Ebel GD, Kramer LD (2007) A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg 77:365–370

    Article  CAS  Google Scholar 

  92. Stapleford KA, Coffey LL, Lay S, Borderia AV, Duong V, Isakov O, Rozen-Gagnon K, Arias-Goeta C, Blanc H, Beaucourt S, Haliloglu T, Schmitt C, Bonne I, Ben-Tal N, Shomron N, Failloux AB, Buchy P, Vignuzzi M (2014) Emergence and transmission of arbovirus evolutionary intermediates with epidemic potential. Cell Host Microbe 15:706–716

    Article  CAS  Google Scholar 

  93. Severini F, Boccolini D, Fortuna C, Di Luca M, Toma L, Amendola A, Benedetti E, Minelli G, Romi R, Venturi G, Rezza G, Remoli ME (2018) Vector competence of Italian Aedes albopictus populations for the chikungunya virus (E1-226V). PLoS Negl Trop Dis 12:e0006435

    Article  Google Scholar 

  94. Vazeille M, Moutailler S, Coudrier D, Rousseaux C, Khun H, Huerre M, Thiria J, Dehecq JS, Fontenille D, Schuffenecker I, Despres P, Failloux AB (2007) Two chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS One 2:e1168

    Article  Google Scholar 

  95. Arias-Goeta C, Mousson L, Rougeon F, Failloux AB (2013) Dissemination and transmission of the E1-226V variant of chikungunya virus in Aedes albopictus are controlled at the midgut barrier level. PLoS One 8:e57548

    Article  CAS  Google Scholar 

  96. Sam IC, Loong SK, Michael JC, Chua CL, Wan Sulaiman WY, Vythilingam I, Chan SY, Chiam CW, Yeong YS, AbuBakar S, Chan YF (2012) Genotypic and phenotypic characterization of chikungunya virus of different genotypes from Malaysia. PLoS One 7:e50476

    Article  CAS  Google Scholar 

  97. Agarwal A, Sharma AK, Sukumaran D, Parida M, Dash PK (2016) Two novel epistatic mutations (E1:K211E and E2:V264A) in structural proteins of chikungunya virus enhance fitness in Aedes aegypti. Virology 497:59–68

    Article  CAS  Google Scholar 

  98. Tsetsarkin KA, Weaver SC (2011) Sequential adaptive mutations enhance efficient vector switching by chikungunya virus and its epidemic emergence. PLoS Pathog 7:e1002412

    Article  CAS  Google Scholar 

  99. Fortuna C, Toma L, Remoli ME, Amendola A, Severini F, Boccolini D, Romi R, Venturi G, Rezza G, Di Luca M (2018) Vector competence of Aedes albopictus for the Indian Ocean lineage (IOL) chikungunya viruses of the 2007 and 2017 outbreaks in Italy: a comparison between strains with and without the E1:A226V mutation. Euro Surveill 23:1800246

    Article  Google Scholar 

  100. de Lamballerie X, Leroy E, Charrel RN, Ttsetsarkin K, Higgs S, Gould EA (2008) Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? Virol J 5:33

    Article  Google Scholar 

  101. Ng LC, Hapuarachchi HC (2010) Tracing the path of chikungunya virus-evolution and adaptation. Infect Genet Evol 10:876–885

    Article  Google Scholar 

  102. Tsetsarkin KA, Chen R, Leal G, Forrester N, Higgs S, Huang J, Weaver SC (2011) Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc Natl Acad Sci USA 108:7872–7877

    Article  CAS  Google Scholar 

  103. Tsetsarkin KA, McGee CE, Volk SM, Vanlandingham DL, Weaver SC, Higgs S (2009) Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS One 4:e6835

    Article  Google Scholar 

  104. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM (2014) The evolution and genetics of virus host shifts. PLoS Pathog 10:e1004395

    Article  Google Scholar 

  105. Pepin KM, Lass S, Pulliam JR, Read AF, Lloyd-Smith JO (2010) Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat Rev Microbiol 8:802–813

    Article  CAS  Google Scholar 

  106. Tsetsarkin KA, Chen R, Yun R, Rossi SL, Plante KS, Guerbois M, Forrester N, Perng GC, Sreekumar E, Leal G, Huang J, Mukhopadhyay S, Weaver SC (2014) Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat Commun 5:4084

    Article  CAS  Google Scholar 

  107. Niyas KP, Abraham R, Unnikrishnan RN, Mathew T, Nair S, Manakkadan A, Issac A, Sreekumar E (2010) Molecular characterization of chikungunya virus isolates from clinical samples and adult Aedes albopictus mosquitoes emerged from larvae from Kerala, South India. Virol J 7:189

    Article  Google Scholar 

  108. Vega-Rua A, Zouache K, Girod R, Failloux AB, Lourenco-de-Oliveira R (2014) High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of chikungunya virus. J Virol 88:6294–6306

    Article  CAS  Google Scholar 

  109. Maljkovic Berry I, Eyase F, Pollett S, Konongoi SL, Joyce MG, Figueroa K, Ofula V, Koka H, Koskei E, Nyunja A, Mancuso JD, Jarman RG, Sang R (2019) Global outbreaks and origins of a chikungunya virus variant carrying mutations which may increase fitness for Aedes aegypti: revelations from the 2016 Mandera, Kenya outbreak. Am J Trop Med Hyg 100:1249–1257

    Article  Google Scholar 

  110. Agha SB, Chepkorir E, Mulwa F, Tigoi C, Arum S, Guarido MM, Ambala P, Chelangat B, Lutomiah J, Tchouassi DP, Turell MJ, Sang R (2017) Vector competence of populations of Aedes aegypti from three distinct cities in Kenya for chikungunya virus. PLoS Negl Trop Dis 11:e0005860

    Article  Google Scholar 

  111. Patil J, More A, Patil P, Jadhav S, Newase P, Agarwal M, Amdekar S, Raut CG, Parashar D, Cherian SS (2018) Genetic characterization of chikungunya viruses isolated during the 2015–2017 outbreaks in different states of India, based on their E1 and E2 genes. Arch Virol 163:3135–3140

    Article  CAS  Google Scholar 

  112. Eyase F, Langat S, Berry IM, Mulwa F, Nyunja A, Mutisya J, Owaka S, Limbaso S, Ofula V, Koka H, Koskei E, Lutomiah J, Jarman RG, Sang R (2020) Emergence of a novel chikungunya virus strain bearing the E1:V80A substitution, out of the Mombasa, Kenya 2017–2018 outbreak. PLoS One 15:e0241754

    Article  CAS  Google Scholar 

  113. Shrinet J, Jain S, Sharma A, Singh SS, Mathur K, Rana V, Bhatnagar RK, Gupta B, Gaind R, Deb M, Sunil S (2012) Genetic characterization of chikungunya virus from New Delhi reveal emergence of a new molecular signature in Indian isolates. Virol J 9:100

    Article  CAS  Google Scholar 

  114. Wangchuk S, Chinnawirotpisan P, Dorji T, Tobgay T, Dorji T, Yoon IK, Fernandez S (2013) Chikungunya fever outbreak, Bhutan, 2012. Emerg Infect Dis 19:1681–1684

    Article  Google Scholar 

  115. Sourisseau M, Schilte C, Casartelli N, Trouillet C, Guivel-Benhassine F, Rudnicka D, Sol-Foulon N, Le Roux K, Prevost MC, Fsihi H, Frenkiel MP, Blanchet F, Afonso PV, Ceccaldi PE, Ozden S, Gessain A, Schuffenecker I, Verhasselt B, Zamborlini A, Saib A, Rey FA, Arenzana-Seisdedos F, Despres P, Michault A, Albert ML, Schwartz O (2007) Characterization of reemerging chikungunya virus. PLoS Pathog 3:e89

    Article  Google Scholar 

  116. Bordi L, Meschi S, Selleri M, Lalle E, Castilletti C, Carletti F, Chiappini R, Di Caro A, Capobianchi MR (2011) Chikungunya virus isolates with/without A226V mutation show different sensitivity to IFN-a, but similar replication kinetics in non human primate cells. New Microbiol 34:87–91

    CAS  Google Scholar 

  117. Fu JYL, Chua CL, Vythilingam I, Sulaiman WYW, Wong HV, Chan YF, Sam IC (2019) An amino acid change in nsP4 of chikungunya virus confers fitness advantage in human cell lines rather than in Aedes albopictus. J Gen Virol 100:1541–1553

    Article  CAS  Google Scholar 

  118. Harapan H, Michie A, Sasmono RT, Imrie A (2020) Dengue: a minireview. Viruses 12:829

    Article  CAS  Google Scholar 

  119. Ooi EE, Goh KT, Gubler DJ (2006) Dengue prevention and 35 years of vector control in Singapore. Emerg Infect Dis 12:887–893

    Article  Google Scholar 

  120. Naveca FG, Claro I, Giovanetti M, de Jesus JG, Xavier J, Iani FCM, do Nascimento VA, de Souza VC, Silveira PP, Lourenco J, Santillana M, Kraemer MUG, Quick J, Hill SC, Theze J, Carvalho RDO, Azevedo V, Salles F, Nunes MRT, Lemos PDS, Candido DDS, Pereira GC, Oliveira MAA, Meneses CAR, Maito RM, Cunha C, Campos DPS, Castilho MDC, Siqueira T, Terra TM, de Albuquerque CFC, da Cruz LN, Abreu AL, Martins DV, Simoes D, Aguiar RS, Luz SLB, Loman N, Pybus OG, Sabino EC, Okumoto O, Alcantara LCJ, Faria NR (2019) Genomic, epidemiological and digital surveillance of chikungunya virus in the Brazilian Amazon. PLoS Negl Trop Dis 13:e0007065

    Article  Google Scholar 

  121. Hapuarachchi HC, Bandara KB, Sumanadasa SD, Hapugoda MD, Lai YL, Lee KS, Tan LK, Lin RT, Ng LF, Bucht G, Abeyewickreme W, Ng LC (2010) Re-emergence of chikungunya virus in South-east Asia: virological evidence from Sri Lanka and Singapore. J Gen Virol 91:1067–1076

    Article  CAS  Google Scholar 

  122. de Lima STS, de Souza WM, Cavalcante JW, da Silva Candido D, Fumagalli MJ, Carrera JP, Simoes Mello LM, De Carvalho Araujo FM, Cavalcante Ramalho IL, de Almeida Barreto FK, de Melo Braga DN, Simiao AR, Miranda da Silva MJ, Alves Barbosa Oliveira RM, Lima CPS, de Sousa Lins C, Barata RR, Pereira Melo MN, Caldas de Souza MP, Franco LM, Fernandes Tavora FR, Queiroz Lemos DR, de Alencar CHM, de Jesus R, de Souza Fonseca V, Dutra LH, de Abreu AL, Lima Araujo EL, Ribas Freitas AR, Vianez Junior J, Pybus OG, Figueiredo LTM, Faria NR, Nunes MRT, Cavalcanti LPG, Miyajima F (2021) Fatal Outcome of chikungunya virus infection in Brazil. Clin Infect Dis 73:e2436–e2443

    Article  Google Scholar 

  123. Simon F, Parola P, Grandadam M, Fourcade S, Oliver M, Brouqui P, Hance P, Kraemer P, Mohamed AA, de Lamballerie X, Charrel R, Tolou H (2007) Chikungunya infection: an emerging rheumatism among travelers returned from Indian Ocean islands. Report of 47 cases. Medicine (Baltim) 86:123–137

    Article  Google Scholar 

  124. Teo TH, Her Z, Tan JJ, Lum FM, Lee WW, Chan YH, Ong RY, Kam YW, Leparc-Goffart I, Gallian P, Renia L, de Lamballerie X, Ng LF (2015) Caribbean and La Reunion chikungunya virus isolates differ in their capacity to induce proinflammatory Th1 and NK cell responses and acute joint pathology. J Virol 89:7955–7969

    Article  CAS  Google Scholar 

  125. Ng LC, Tan LK, Tan CH, Tan SS, Hapuarachchi HC, Pok KY, Lai YL, Lam-Phua SG, Bucht G, Lin RT, Leo YS, Tan BH, Han HK, Ooi PL, James L, Khoo SP (2009) Entomologic and virologic investigation of chikungunya, Singapore. Emerg Infect Dis 15:1243–1249

    Article  Google Scholar 

  126. Huang JH, Yang CF, Su CL, Chang SF, Cheng CH, Yu SK, Lin CC, Shu PY (2009) Imported chikungunya virus strains, Taiwan, 2006–2009. Emerg Infect Dis 15:1854–1856

    Article  Google Scholar 

  127. Auerswald H, Boussioux C, In S, Mao S, Ong S, Huy R, Leang R, Chan M, Duong V, Ly S, Tarantola A, Dussart P (2018) Broad and long-lasting immune protection against various chikungunya genotypes demonstrated by participants in a cross-sectional study in a Cambodian rural community. Emerg Microbes Infect 7:13

    Article  Google Scholar 

  128. Langsjoen RM, Haller SL, Roy CJ, Vinet-Oliphant H, Bergren NA, Erasmus JH, Livengood JA, Powell TD, Weaver SC, Rossi SL (2018) Chikungunya virus strains show lineage-specific variations in virulence and cross-protective ability in murine and nonhuman primate models. mBio 9:e02449

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the staff of Klinik Bahasa in the Office of Research and Publication, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia, for critical reading of this manuscript; Resti Yudhiyanti (Center for Child Health-Pediatric Research Office [PKKA-PRO]) for her technical assistance; and Adam Ash Shidiq for his expert assistance in preparing the figures.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, 55281, Indonesia

    Mohamad S. Hakim, Luthvia Annisa & Abu T. Aman

  2. Master Program in Biotechnology, Postgraduate School, Universitas Gadjah Mada, Yogyakarta, Indonesia

    Faris M. Gazali

Authors
  1. Mohamad S. Hakim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luthvia Annisa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Faris M. Gazali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abu T. Aman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M. S. H. was involved in conceptualization, writing the original draft, editing, and finalization. L. A., F. M. G., and A. T. A. were involved in editing and finalization. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Mohamad S. Hakim.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest. The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Additional information

Handling Editor: Patricia Aguilar.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hakim, M.S., Annisa, L., Gazali, F.M. et al. The origin and continuing adaptive evolution of chikungunya virus. Arch Virol 167, 2443–2455 (2022). https://doi.org/10.1007/s00705-022-05570-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05570-z

Search

Navigation